Long-term inhibitory plasticity in visual cortical layer 4 switches sign at the opening of the critical period

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 47, 2013, Pages

  Lefort, Sandrine ^a   Gray, Annette C ^a,b   Turrigiano, Gina G ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; LONG TERM POTENTIATION; MOUSE; NEGATIVE FEEDBACK; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; STRIATE CORTEX; SYNAPSE; VISUAL CORTEX;

FS CELL; LTD; LTP;

ANIMALS; CRITICAL PERIOD (PSYCHOLOGY); GABAERGIC NEURONS; LONG-TERM POTENTIATION; NEURAL PATHWAYS; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; RATS; STATISTICS, NONPARAMETRIC; SYNAPSES; VISUAL CORTEX;

EID: 84888107646     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1319571110     Document Type: Article

References (52)

1. Hubel DH, Wiesel TN, LeVay S (1977) Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc Lond B Biol Sci 278(961-377-409.
2. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274(5290-1133-1138.
3. Desai NS, Cudmore RH, Nelson SB, Turrigiano GG (2002) Critical periods for experience- dependent synaptic scaling in visual cortex. Nat Neurosci 5(8-783-789.
4. Li Y, Fitzpatrick D, White LE (2006) The development of direction selectivity in ferret visual cortex requires early visual experience. Nat Neurosci 9(5-676-681.
5. Smith SL, Trachtenberg JT (2007) Experience-dependent binocular competition in the visual cortex begins at eye opening. Nat Neurosci 10(3-370-375.
6. Feller MB, Scanziani M (2005) A precritical period for plasticity in visual cortex. Curr Opin Neurobiol 15(1-94-100.
7. Hensch TK (2004) Critical period regulation. Annu Rev Neurosci 27:549-579.
8. Hooks BM, Chen C (2007) Critical periods in the visual system: Changing views for a model of experience-dependent plasticity. Neuron 56(2-312-326.
9. Maffei A, Turrigiano G (2008) The age of plasticity: Developmental regulation of synaptic plasticity in neocortical microcircuits. Prog Brain Res 169:211-223.
10. Fagiolini M, et al. (2004) Specific GABAA circuits for visual cortical plasticity. Science 303(5664-1681-1683.
11. Hensch TK (2005) Critical period plasticity in local cortical circuits. Nat Rev Neurosci 6(11-877-888.
12. Chattopadhyaya B, et al. (2004) Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24(43-9598-9611.
13. Chattopadhyaya B, et al. (2007) GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 54(6-889-903.
14. Di Cristo G, et al. (2004) Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs. Nat Neurosci 7(11- 1184-1186.
15. Fagiolini M, Hensch TK (2000) Inhibitory threshold for critical-period activation in primary visual cortex. Nature 404(6774-183-186.
16. Hensch TK, et al. (1998) Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282(5393-1504-1508.
17. Iwai Y, Fagiolini M, Obata K, Hensch TK (2003) Rapid critical period induction by tonic inhibition in visual cortex. J Neurosci 23(17-6695-6702.
18. Maffei A, Nelson SB, Turrigiano GG (2004) Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat Neurosci 7(12-1353-1359.
19. Maffei A, Nataraj K, Nelson SB, Turrigiano GG (2006) Potentiation of cortical inhibition by visual deprivation. Nature 443(7107-81-84.
20. Dunning DD, Hoover CL, Soltesz I, Smith MA, O'Dowd DK (1999) GABA(A) receptormediated miniature postsynaptic currents and alpha-subunit expression in developing cortical neurons. J Neurophysiol 82(6-3286-3297.
21. Fritschy JM, Paysan J, Enna A, Mohler H (1994) Switch in the expression of rat GABAAreceptor subtypes during postnatal development: An immunohistochemical study. J Neurosci 14(9-5302-5324.
22. Laurie DJ, Wisden W, Seeburg PH (1992) The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 12(11-4151-4172.
23. Trigo FF, Chat M, Marty A (2007) Enhancement of GABA release through endogenous activation of axonal GABA(A) receptors in juvenile cerebellum. J Neurosci 27(46- 12452-12463.
24. Malinow R, Tsien RW (1990) Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 346(6280-177-180.
25. Castillo PE, Chiu CQ, Carroll RC (2011) Long-term plasticity at inhibitory synapses. Curr Opin Neurobiol 21(2-328-338.
26. Komatsu Y (1996) GABAB receptors, monoamine receptors, and postsynaptic inositol trisphosphate-induced Ca2+ release are involved in the induction of long-term potentiation at visual cortical inhibitory synapses. J Neurosci 16(20-6342-6352.
27. Jiang B, Sohya K, Sarihi A, Yanagawa Y, Tsumoto T (2010) Laminar-specific maturation of GABAergic transmission and susceptibility to visual deprivation are related to endocannabinoid sensitivity in mouse visual cortex. J Neurosci 30(42-14261-14272.
28. Markram H, et al. (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5(10-793-807.
29. Ascoli GA, et al.; Petilla Interneuron Nomenclature Group (2008) Petilla terminology: Nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9(7-557-568.
30. Isaacson JS, Scanziani M (2011) How inhibition shapes cortical activity. Neuron 72(2- 231-243.
31. Moore CI, Carlen M, Knoblich U, Cardin JA (2010) Neocortical interneurons: From diversity, strength. Cell 142(2-189-193.
32. Vogels TP, Abbott LF (2009) Gating multiple signals through detailed balance of excitation and inhibition in spiking networks. Nat Neurosci 12(4-483-491.
33. Vogels TP, Sprekeler H, Zenke F, Clopath C, Gerstner W (2011) Inhibitory plasticity balances excitation and inhibition in sensory pathways and memory networks. Science 334(6062-1569-1573.
34. Yizhar O, et al. (2011) Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477(7363-171-178.
35. House DR, Elstrott J, Koh E, Chung J, Feldman DE (2011) Parallel regulation of feedforward inhibition and excitation during whisker map plasticity. Neuron 72(5- 819-831.
36. Kullmann DM, Lamsa KP (2011) LTP and LTD in cortical GABAergic interneurons: Emerging rules and roles. Neuropharmacology 60(5-712-719.
37. Kullmann DM, Moreau AW, Bakiri Y, Nicholson E (2012) Plasticity of inhibition. Neuron 75(6-951-962.
38. Luscher B, Fuchs T, Kilpatrick CL (2011) GABAA receptor trafficking-mediated plasticity of inhibitory synapses. Neuron 70(3-385-409.
39. McBain CJ, Kauer JA (2009) Presynaptic plasticity: Targeted control of inhibitory networks. Curr Opin Neurobiol 19(3-254-262.
40. Komatsu Y, Iwakiri M (1993) Long-term modification of inhibitory synaptic transmission in developing visual cortex. Neuroreport 4(7-907-910.
41. Nugent FS, Penick EC, Kauer JA (2007) Opioids block long-term potentiation of inhibitory synapses. Nature 446(7139-1086-1090.
42. Brown TE, Chirila AM, Schrank BR, Kauer JA (2013) Loss of interneuron LTD and attenuated pyramidal cell LTP in Trpv1 and Trpv3 KO mice. Hippocampus 23(8-662-671.
43. Komatsu Y (1994) Age-dependent long-term potentiation of inhibitory synaptic transmission in rat visual cortex. J Neurosci 14(11 Pt 1-6488-6499.
44. Kotak VC, Sanes DH (2000) Long-lasting inhibitory synaptic depression is age- and calcium-dependent. J Neurosci 20(15-5820-5826.
45. McLean HA, Caillard O, Ben-Ari Y, Gaiarsa JL (1996) Bidirectional plasticity expressed by GABAergic synapses in the neonatal rat hippocampus. J Physiol 496(Pt 2-471-477.
46. Luhmann HJ, Prince DA (1991) Postnatal maturation of the GABAergic system in rat neocortex. J Neurophysiol 65(2-247-263.
47. Malenka RC, Bear MF (2004) LTP and LTD: An embarrassment of riches. Neuron 44(1-5-21.
48. Sáez I, Friedlander MJ (2009) Plasticity between neuronal pairs in layer 4 of visual cortex varies with synapse state. J Neurosci 29(48-15286-15298.
49. Philpot BD, Cho KK, Bear MF (2007) Obligatory role of NR2A for metaplasticity in visual cortex. Neuron 53(4-495-502.
50. Turrigiano G (2011) Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. Annu Rev Neurosci 34:89-103.
51. Cruikshank SJ, Urabe H, Nurmikko AV, Connors BW (2010) Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron 65(2-230-245.
52. Wang L, Kloc M, Gu Y, Ge S, Maffei A (2013) Layer-specific experience-dependent rewiring of thalamocortical circuits. J Neurosci 33(9-4181-4191.